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SHORT REPORT Open Access A high-intensity cluster of Schistosoma mansoni infection around Mbita causeway, western Kenya: a confirmatory cross- sectional survey Evans Asena Chadeka 1,2,3 , Sachiyo Nagi 2,3 , Ngetich B. Cheruiyot 4 , Felix Bahati 4 , Toshihiko Sunahara 3,5 , Sammy M. Njenga 6 and Shinjiro Hamano 1,2,3,4* Abstract In Kenya, communities residing along the shores and islands of Lake Victoria bear a substantial burden of schistosomiasis. Although there is a school-based deworming program in place, the transmission of Schistosoma mansoni varies even at a fine scale. Given the focal nature of schistosomestransmission, we aim to identify areas with high intensity of S. mansoni infection in Mbita, Homabay County, western Kenya, for prioritized integrated control measures. Our findings confirm a high intensity of S. mansoni infection cluster around Mbita causeway. While the current efforts to curtail morbidity due to schistosomiasis through preventive chemotherapy in schools are crucial, fine-scale mapping of risk areas is necessary for specific integrated control measures. Keywords: Schistosomiasis, Clustering, Mbita causeway, Western Kenya Introduction Globally, 218 million individuals suffer from schistosom- iasis, while 700 million are at risk in endemic regions [1]. Among the three species commonly causing schisto- somiasis, Schistosoma mansoni, Schistosoma haemato- bium, and Schistosoma japonicum, the former two are occurring in Africa [2]. Six million Kenyans are infected, and another 15 million are at risk of schistosomiasis [3]. Communities residing along the shores and on islands of Lake Victoria bear a major schistosomiasis burden in Kenya [48]. The Kenya national school-based deworming program (NSBDP) was launched in 2009 and schoolchildren were treated for soil-transmitted helminths (STHs). In 2012, NSBDP was scaled up nationally. Schoolchildren in en- demic regions have since been treated for schistosomia- sis and STHs. The national control team with cascaded support at county and sub-county levels coordinates co-administration of albendazole for STHs and prazi- quantel for schistosomiasis. However, some years have witnessed treatment of STHs only due to lack of prazi- quantel for schistosomiasis treatment [9, 10]. Considerable spatial variation in the transmission of schistosomes can be explained by human contact pat- terns to infested water, the presence of competent inter- mediate snail hosts, availability of suitable snail hosts habitats, freshwater environment contamination with stool/urine containing eggs with miracidium, and diver- sity of human hostsimmunity [11]. The highly focal na- ture of schistosomiasis calls for fine-scale mapping of the disease. Accurate information on the distribution of the infection is necessary for prioritized allocation of constrained control resources to populations which are at a higher risk. With the devolvement of health care de- livery at the county level in Kenya, neglected tropical diseases (NTD) control programs are likely to be man- aged at the county level. We purpose to pinpoint S. mansoni infection high transmission areas in Mbita Sub- county of Homabay County for prioritized intervention with a possible replication to other endemic areas. © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. * Correspondence: [email protected] 1 Leading program, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan 2 Department of Parasitology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, Nagasaki, Japan Full list of author information is available at the end of the article Tropical Medicine and Health Chadeka et al. Tropical Medicine and Health (2019) 47:26 https://doi.org/10.1186/s41182-019-0152-y

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  • SHORT REPORT Open Access

    A high-intensity cluster of Schistosomamansoni infection around Mbita causeway,western Kenya: a confirmatory cross-sectional surveyEvans Asena Chadeka1,2,3, Sachiyo Nagi2,3, Ngetich B. Cheruiyot4, Felix Bahati4, Toshihiko Sunahara3,5,Sammy M. Njenga6 and Shinjiro Hamano1,2,3,4*

    Abstract

    In Kenya, communities residing along the shores and islands of Lake Victoria bear a substantial burden ofschistosomiasis. Although there is a school-based deworming program in place, the transmission of Schistosomamansoni varies even at a fine scale. Given the focal nature of schistosomes’ transmission, we aim to identify areaswith high intensity of S. mansoni infection in Mbita, Homabay County, western Kenya, for prioritized integratedcontrol measures. Our findings confirm a high intensity of S. mansoni infection cluster around Mbita causeway.While the current efforts to curtail morbidity due to schistosomiasis through preventive chemotherapy in schoolsare crucial, fine-scale mapping of risk areas is necessary for specific integrated control measures.

    Keywords: Schistosomiasis, Clustering, Mbita causeway, Western Kenya

    IntroductionGlobally, 218 million individuals suffer from schistosom-iasis, while 700 million are at risk in endemic regions[1]. Among the three species commonly causing schisto-somiasis, Schistosoma mansoni, Schistosoma haemato-bium, and Schistosoma japonicum, the former two areoccurring in Africa [2]. Six million Kenyans are infected,and another 15 million are at risk of schistosomiasis [3].Communities residing along the shores and on islands ofLake Victoria bear a major schistosomiasis burden inKenya [4–8].The Kenya national school-based deworming program

    (NSBDP) was launched in 2009 and schoolchildren weretreated for soil-transmitted helminths (STHs). In 2012,NSBDP was scaled up nationally. Schoolchildren in en-demic regions have since been treated for schistosomia-sis and STHs. The national control team with cascaded

    support at county and sub-county levels coordinatesco-administration of albendazole for STHs and prazi-quantel for schistosomiasis. However, some years havewitnessed treatment of STHs only due to lack of prazi-quantel for schistosomiasis treatment [9, 10].Considerable spatial variation in the transmission of

    schistosomes can be explained by human contact pat-terns to infested water, the presence of competent inter-mediate snail hosts, availability of suitable snail hostshabitats, freshwater environment contamination withstool/urine containing eggs with miracidium, and diver-sity of human hosts’ immunity [11]. The highly focal na-ture of schistosomiasis calls for fine-scale mapping ofthe disease. Accurate information on the distribution ofthe infection is necessary for prioritized allocation ofconstrained control resources to populations which areat a higher risk. With the devolvement of health care de-livery at the county level in Kenya, neglected tropicaldiseases (NTD) control programs are likely to be man-aged at the county level. We purpose to pinpoint S.mansoni infection high transmission areas in Mbita Sub-county of Homabay County for prioritized interventionwith a possible replication to other endemic areas.

    © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

    * Correspondence: [email protected] program, Graduate School of Biomedical Sciences, NagasakiUniversity, Nagasaki, Japan2Department of Parasitology, Institute of Tropical Medicine (NEKKEN),Nagasaki University, Nagasaki, JapanFull list of author information is available at the end of the article

    Tropical Medicineand Health

    Chadeka et al. Tropical Medicine and Health (2019) 47:26 https://doi.org/10.1186/s41182-019-0152-y

    http://crossmark.crossref.org/dialog/?doi=10.1186/s41182-019-0152-y&domain=pdfhttp://creativecommons.org/licenses/by/4.0/http://creativecommons.org/publicdomain/zero/1.0/mailto:[email protected]

  • MethodsThis study was conducted in Mbita health demographicsurveillance system (HDSS), a rural setting along theshores and on islands of Lake Victoria, Homabay County,western Kenya [12]. Briefly, Mbita HDSS is comprised ofRusinga on the island and Gembe situated on the main-land. In the early 1980s, Mbita causeway was constructedto enhance linkage between Rusinga Island and mainland.The key sources of livelihoods in the area are fishing, sub-sistence farming, and small-scale trade.By June 2014, Mbita HDSS data showed 5580 children

    (2683 boys and 2897 girls) were enrolled in preschool.We randomly sampled 1200 pre-schoolers based onsample size calculation for finite population [13]. Thissample was proportionately distributed among the 66eligible schools. In September to October 2014, we col-lected stool samples for two sequential days. Sampleswere prepared in duplicate for microscopic examinationof S. mansoni and STHs using Kato-Katz technique [14].S. mansoni infection was categorized as light (1–99 eggsper gram of feces (EPG)), moderate (100–399 EPG), orheavy (≥ 400 EPG) [15]. Pearson’s chi-square test orFisher’s exact test was used to compare infection preva-lence in the four regions of the study area. P value lessthan 0.05 was considered statistically significant. To il-lustrate the clustering of schistosomiasis, we utilizedSaTScan software version 9 [16].

    ResultsWe present findings from 813 preschool children withcomplete parasitological data. The mean age was 5.1 years(range 2–6), 48.7% were boys while 51.3% were girls.

    Table 1 details the prevalence and intensity of S. mansoniinfection and STHs. The overall prevalence of S. mansoniinfection was 45.1% (95% CI, 41.7–48.5). There was a ten-dency in the decline of S. mansoni infection intensity withfurther inland location of participants’ residence from thelake, OR = 0.9989 (95% CI, 0.9987–0.9992). The preva-lence of hookworms, A. lumbricoides, and T. trichiurawas 1.1% (95% CI, 0.4–1.8), 1.8% (95% CI, 0.9–2.8), and1.1% (95% CI, 0.4–1.8) respectively.Both the prevalence and intensity of S. mansoni infec-

    tion were significantly lower in Gembe East compared tothe rest of the study area. In Fig. 1, we observed ahigh-intensity cluster of S. mansoni infection coveringalmost the entire Rusinga Island and the western edge ofGembe close to Mbita causeway. The high-intensitycluster radius was 5.1 km containing 351 participants;the mean inside was 11.6 EPG, while mean outside was2.5 EPG, P = 0.001.

    DiscussionIn this report, we confirmed a high S. mansoni infectionrisk area covering Rusinga Island and the western edgeof Gembe mainland around Mbita causeway (Fig. 1). Wepreviously made this observation, and there was a trendof infection risk decreasing towards the eastern side ofGembe mainland [4]. Our previous study was howeverlimited by the small sample obtained by cluster samplingof schools. In the current study, participants were ran-domly selected from all the eligible schools within thestudy area. Individuals residing near infested watersources are likely to be in frequent contact with infestedwater and hence higher probability of S. mansoni

    Table 1 Prevalence and intensity of S. mansoni and STHs among preschool children in Mbita, western Kenya

    Overall n = 813 Location

    Prevalence (95% CI) Gembe West (n = 244) Gembe East (n = 186) Rusinga West (n = 232) Rusinga East (n = 151) P

    Parasite

    S. mansoni 45.1 (41.7–48.5) 135 (55.3%) 36 (19.4%) 124 (53.4%) 98 (64.9%) < 0.0001a

    Light1 28.9 (25.8–32.0) 60 (24.5%) 29 (15.6%) 86 (37.1%) 60 (39.7%) < 0.0001a

    Moderate2 10.6 (8.4–12.7) 28 (11.3%) 7 (3.8%) 24 (10.3%) 27 (17.9%) < 0.0001a

    Heavy3 5.7 (4.1–7.3) 21 (8.6%) 0 (0.0%) 14 (6.0%) 11 (7.3%) < 0.0001b

    STHs

    Hookworm 1.1 (0.4–1.8) 4 (1.6%) 2 (1.1%) 0 (0.0%) 2 (1.3%) 0.1516b

    A. lumbricoides 1.8 (0.9–2.8) 5 (2.0%) 3 (1.6%) 2 (0.9%) 5 (3.3%) 0.3641b

    T. trichiura 1.1 (0.4–1.8) 2 (0.8%) 2 (1.1%) 3 (1.3%) 2 (1.3%) 0.9383b

    Residence location

    Near (< 508.1 m)4 406 (49.9%) 121 (49.5%) 60 (32.3%) 125 (53.9%) 103 (68.2%) < 0.0001a

    11–99 eggs per gram of feces (EPG)2100–399 EPG3≥ 400 EPG4Participant’s residence distance to lakeshore grouped into near, i.e., < 508.1 m based on median distanceaChi-square testbFisher’s exact test

    Chadeka et al. Tropical Medicine and Health (2019) 47:26 Page 2 of 4

  • infection [11]. Based on the current data, the reason forhigh prevalence and intensity of S. mansoni in Gembewest and Rusinga Island is that the majority of partici-pants were residing close to the lakeshore (55.7%) com-pared to those in Gembe East (32.3%). Secondly, wepreviously demonstrated that the high population dens-ity around Mbita causeway was associated with high S.mansoni infection risk. This can be explained in termsof the transmission dynamics of the parasite. In poor hy-giene settings, host snails get infected with S. mansonidue to water environment pollution with feces contain-ing S. mansoni eggs. The parasite prevalence among thehost snails is dependent on absolute numbers of infectedindividuals and not S. mansoni prevalence among thehuman population [4]. Schistosomiasis control programsutilizing mass drug administration (MDA) with prazi-quantel have managed to bring down disease-relatedmorbidity and prevalence in endemic regions. However,some settings have maintained high levels of intensityand prevalence despite MDA [17–20]. In areas wheremorbidity has been lowered, MDA has to be comple-mented with other measures including improvement ofaccess to safe water and proper sanitation coupled withsnail control to avoid resurgence of disease transmission.Fine-scale mapping of the disease transmission is para-mount for identifying persistent high-risk areas and

    prudent allocation of limited control resources. This willbe necessary as national control programs reduce mor-bidity, and prevalence in endemic areas and spatial pat-terns in turn are more heterogeneous [21].This study had a weakness of not investigating S. man-

    soni infection in intermediate host snails and not asses-sing human behavioral and environmental factorsassociated with S. mansoni infection risk. Irrespective ofthe mentioned shortcomings, our current reportre-emphasizes high schistosomiasis risk in Mbita alongthe shores and on islands of Lake Victoria. We have sin-gled out the high-risk areas, and this will go a long wayin prioritizing integrated control efforts based onarea-specific needs geared towards reduction of S. man-soni morbidity and mortality.

    AbbreviationsCI: Confidence interval; EPG: Eggs per gram; HDSS: Health demographicsurveillance system; MDA: Mass drug administration; NSBDP: National school-based deworming program; NTD: Neglected tropical disease; OR: Odds ratio;STH: Soil-transmitted helminth; WHO: World Health Organization

    AcknowledgmentsWe appreciate the director of the Kenya Medical Research Institute (KEMRI)for collaborative support. Our sincere gratitude goes to the children, parents/guardians, and teachers who willingly took part in this study. We wish tothank management teams of Mbita sub-county health and education depart-ments for their collaborative support. We are grateful to Mbita HDSS teamfor guiding us during our field activities. We are beholden to: Yoshio

    Fig. 1 High-intensity cluster of S. mansoni infection among preschool children in Mbita, western Kenya. The small white, yellow, green, and reddots depict the location of negative, light, moderate, and heavy cases respectively. The red dotted circle shows the S. mansoni infectionhigh-intensity cluster

    Chadeka et al. Tropical Medicine and Health (2019) 47:26 Page 3 of 4

  • Ichinose, Yukie Saito, Sizuko Yagi, Masae Ishiguru, Yasuko Kawabata, andChiaki Hisata for administrative support, members of Parasitology Depart-ment, Nagasaki University for helpful discussion.

    FundingThis study was supported by Strategic Young Researcher Overseas VisitsProgram for Accelerating Brain Circulation 2013–2015 by JSPS (S2509 toShinjiro Hamano) and a Grants-in-Aid for International Scientific Research (A)by JSPS (17H01684 to Shinjiro Hamano). This work was conducted at theJoint Usage/Research Center on Tropical Disease, Institute of Tropical Medi-cine, Nagasaki University. Evans Asena Chadeka received a PhD scholarshipfrom Leading Program, Graduate School of Biomedical Sciences, NagasakiUniversity. Sachiyo Nagi was supported by Japan Society for Promotion ofScience (JSPS) as a research fellow (Research Fellowship for Young ScientistsDC2, PD). The funders had no role in study design, data collection and ana-lysis, decision to publish, or preparation of the manuscript.

    Availability of data and materialsData set used for this report can be availed by the corresponding author onreasonable request.

    Authors’ contributionsSH, SN, and EAC conceptualized and designed the study. NBC, SN, FB, andEAC collected and analyzed the data. EAC drafted the manuscript. SMN, TS,and SH edited and critically revised the manuscript. All authors read andapproved the final version of the manuscript.

    Ethics approval and consent to participateThe ethical review unit of KEMRI reviewed and approved this study (SERUNo. 3092), and ethical review board of Institute of Tropical Medicine,Nagasaki University, Japan (No. 10121666). All parents/guardians gave awritten consent while the preschool children ascended to the study.

    Consent for publicationPublication for this report was authorized by the director KEMRI.

    Competing interestsThe authors declare that they have no competing interests.

    Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.

    Author details1Leading program, Graduate School of Biomedical Sciences, NagasakiUniversity, Nagasaki, Japan. 2Department of Parasitology, Institute of TropicalMedicine (NEKKEN), Nagasaki University, Nagasaki, Japan. 3The Joint Usage/Research Center on Tropical Diseases, Institute of Tropical Medicine(NEKKEN), Nagasaki University, Nagasaki, Japan. 4Nagasaki University, KenyaResearch Station, NUITM-KEMRI Project, Nairobi, Kenya. 5Department ofVector Ecology and Environment, Institute of Tropical Medicine (NEKKEN),Nagasaki University, Nagasaki, Japan. 6Eastern and Southern Africa Centre ofInternational Parasite Control (ESACIPAC), Kenya Medical Research Institute(KEMRI), Nairobi, Kenya.

    Received: 30 January 2019 Accepted: 21 March 2019

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    AbstractIntroductionMethodsResultsDiscussionAbbreviationsAcknowledgmentsFundingAvailability of data and materialsAuthors’ contributionsEthics approval and consent to participateConsent for publicationCompeting interestsPublisher’s NoteAuthor detailsReferences